Papel-de-los-colembolos-en-los-procesos-de-descomposicion-de-hojarasca-en-los-manglares--el-caso-de-la-Isla-de-Cozumel-Quintana-Roo-Mexico

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UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO 
POSGRADO EN CIENCIAS BIOLÓGICAS 
FACULTAD DE CIENCIAS, UNAM 
ECOLOGÍA 
 
 
PAPEL DE LOS COLÉMBOLOS EN LOS PROCESOS DE DESCOMPOSICIÓN EN LOS 
MANGLARES: EL CASO DE COZUMEL, QUITANA ROO, MÉXICO 
TESIS 
QUE PARA OPTAR POR EL GRADO DE: 
DOCTOR EN CIENCIAS 
 
 
PRESENTA: 
ARTURO GARCÍA GÓMEZ 
 
 
 
TUTOR PRINCIPAL DE TESIS: DRA. ROSA GABRIELA CASTAÑO MENESES, FACULTAD DE CIENCIAS, UNAM 
COMITÉ TUTOR: DR. JOSÉ GUADALUPE PALACIOS VARGAS, FACULTAD DE CIENCIAS, UNAM 
 DR. ATILANO CONTRERAS RAMOS, INSTITUTO DE BIOLOGÍA, UNAM 
 
 
 
MÉXICO, D.F. MAYO 2015 
 
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UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO 
POSGRADO EN CIENCIAS BIOLÓGICAS 
FACULTAD DE CIENCIAS, UNAM 
ECOLOGÍA 
 
 
PAPEL DE LOS COLÉMBOLOS EN LOS PROCESOS DE DESCOMPOSICIÓN EN LOS 
MANGLARES: EL CASO DE COZUMEL, QUITANA ROO, MÉXICO 
TESIS 
QUE PARA OPTAR POR EL GRADO DE: 
DOCTOR EN CIENCIAS 
 
 
PRESENTA: 
ARTURO GARCÍA GÓMEZ 
 
 
 
TUTOR PRINCIPAL DE TESIS: DRA. ROSA GABRIELA CASTAÑO MENESES, FACULTAD DE CIENCIAS, UNAM 
COMITÉ TUTOR: DR. JOSÉ GUADALUPE PALACIOS VARGAS, FACULTAD DE CIENCIAS, UNAM 
 DR. ATILANO CONTRERAS RAMOS, INSTITUTO DE BIOLOGÍA, UNAM 
 
 
 
MÉXICO, D.F. MAYO 2015 
V~IV~OAD NAqOHAL 
Av1"1tMA DE 
MrxIC,O 
Dr. Isidro Ávlla Martinez 
POSGRADO EN CIENCIAS BIOLÓGICAS 
FACULTAD DE CIENCIAS 
DIVISiÓN DE ESTUDIOS DE POSGRADO 
OFICIO FCIElDEPI186115 
ASUNTO: Oficio de Jurado 
Director General de Administración Escolar, UNAM 
Presente 
Me permito informar a usted que en la reunión ordinaria del Comité Académico del Posgrado en 
Ciencias Bíol6gicas. celebrada el dia 9 de f.brero de 2015, se aprobó el sigu iente jurado para el 
examen de grado de DOCTOR EN CIENCIAS del (la) alumno (a) GARCIA GÓMEZ ARTURO con número 
de cuenta 94106592 con la tesis titulada : "Papel de los co"mboloa en loa procesos de descomposición 
en los m.ngl.res: e' caso de la 1. 1. de Cozumel , Qulntan. Roo, M6xlco" , realizada bajo la dirección del 
(la) DRA. ROSA GABRIELA CASTAÑO MENESES: 
Presidente: 
Vocal: 
Secretario: 
Suplente' 
Suplente 
DR. EFRAiN lOVAR SANCHEZ 
DRA. ALICIA CAlLEJAS CHAVERO 
DR. JOS~ GUADALUPE PALACIOS VARGAS 
DR. SANTIAGO ZARAGOZA CABALLERO 
DR. ALFONSO NERI GARclA ALDRETE 
Sin otro particular, me es grato enviarle un cordial saludo. 
~,..o DE 01. 
Atentamente V" U~1< 
·POR MI RAZA HABLARA EL ESP/RITU· O . O 
Cd. Universitaria, D.F. a 18 de marzo de 2015. ~ '; 
JIt. JJ G.o f7 JAn m -DIVISION oe':sruo~ 
Dra. Maria del Coro Arizm~ri:;'; DE POSQRAOQ 
Coordinadora del Programa 
MCAAlMJFMlASRllpp 
Agradecimientos 
Al posgrado de Ciencias Biológicas, UNAM por todo el apoyo proporcionado para efectuar 
los estudios en el programa de Doctorado, área de ecología. 
Al CONACyT por el apoyo de la beca proporcionada para continuar mis estudios de 
posgrado en el programa doctoral de la Facultad de Ciencias, UNAM. 
A la Facultad de Ciencias, UNAM por el apoyo logístico al presentar los trabajos derivados 
del proyecto de investigación del doctorado en el XIIIth International Colloquium on 
Apterygota, y XVIth International Colloquium on Soil Zoology, ambos en Coimbra, 
Portugal. 
A la Dra. Gabriela Castaño Meneses, directora de esta tesis, por su ayuda, apoyo, confianza 
y amistad que siempre me brindo durante mi desarrollo y formación académica. 
A los Drs. Gabriela Castaño Meneses, José Guadalupe Palacios Vargas y Atilano Contreras 
Ramos, miembros del comité tutoral, quienes siempre estuvieron presentes para plantear las 
interrogantes y ayudarme a encontrar las soluciones para éstas. 
Al Dr. Palacios Vargas, quien desinteresadamente estuvo la pendiente de mi desarrollo 
mediante la revisión de los manuscritos, y sus valiosos comentarios que enriquecieron a la 
misma. 
A los Drs. Alicia Callejas Chavero, Efraín Tovar Sánchez, Santiago Zaragoza Caballero y 
Alfonso Neri García Aldrete, quienes revisaron e hicieron importantes aportes al escrito final, 
así como formaron parte importante en mi formación como Dr. en Ciencias. 
 
Dedicatorias 
A mi MADRE † 
A Lourdes Anastasio Gonzales, mi mejor amiga y cordada de vida. 
A mis hermanos, Sandra y Luís (se llama Chino, le decimos Luís), quienes siempre me han 
acompañado en mis locuras. 
A mi familia en general, somos tantos que sería injusto se me olvidara alguien. 
A mis compañeros de laboratorio de Microartrópodos, ustedes pueden chavos; si yo pude, 
ustedes también pueden, particularmente a Daniela, Isaac, Elihú y Carmén quienes hacen del 
mundo un lugar más agradable. 
A la Dra Blanca Estela Mejía Recamier, por su sincera amistad y sus ricos panes. 
Índice general 
Resumen 1 
Abstract 2 
1. Introducción 3 
1.1 Collembola 3 
1.2 Adaptaciones de Collembola al medio litoral 4 
1.3 Ecosistema tropical 5 
1.4 Collembola y el medio litoral 6 
1.5 Degradación de la materia orgánica 7 
1.6 Colémbolos y la degradación de la materia orgánica del suelo 8 
2. Justificación 9 
3. Resumen de capítulos 10 
Capítulo I: 
Mesofaunal arthropod diversity in shrub mangrove litter f Cozumel 
Island, Quintana Roo, México 
 
12 
Capítulo II: 
Diversity and distribution of Collembola (Hexapoda) in two mangroves, in 
Punta Sur, Cozumel, Mexico 
 
19 
Capitulo III: 
Cambios en la degradación de hojarasca de Rhizophora mangle L. bajo 
diferentes tipos de interacciones de Xenylla pseudomaritima 
 
38 
4. Conclusiones finales 56 
5. Bibliografía 57 
 
 
 
1 
 
Resumen 
Los Collembola junto con los Oribatida, son dos grupos importantes de artrópodos que 
conforman la mesofauna edáfica, cuyas comunidades han sido estudiadas en bosques 
templados y selvas; sin embargo, en los manglares continentales o de isla, se cuenta con poca 
información, en particular en México, donde la artrópodofauna de estos ambientes es 
prácticamente desconocida. 
México presenta un territorio extenso y de gran biodiversidad, con grandes extensiones 
de zonas con manglar a lo largo del país, dichas áreas presentan diferencias que van desde la 
vegetación que la compone, hasta la geomorfología. 
En el caso de Cozumel, particularmente en el sur, podemos encontrar una vegetación 
dominada por Rhizophora mangle y Avicennia nitida, dichos árboles se encuentran rodeando 
diferentes lagunas, las cuales sólo son inundables en época de lluvias, además al estar 
alejadas del mar se consideran como una manglar seco. 
Antes del presente estudio, no se conocían los artrópodos de la mesofauna edáfica que 
integran los manglares de Cozumel, actualmente se registraron 30 órdenes, siendo los más 
abundantes Oribatida y Collembola. 
En el caso de los colémbolos, se registraron 53 taxones, siendo Lepidocyrtus ca. 
floridensis, Hemisotoma thermophila y Xenylla yucatana, los de mayor densidad 
poblacional; de igual forma se observó un marcado efecto estacional y de temperatura, sobre 
la estructura de las comunidad de Collembola, principalmente en el manglar de la Laugna 
Colombia, además se registró un recambio de especies entre los manglares estudiados. 
Por otro lado, se ha observado la importancia de la mesofauna en los procesos de 
degradación y fragmentación de la hojarasca, además influyen en la actividad de hongosy 
bacterias, de los que se alimentan; de tal forma que se realizó un estudio en un ambiente 
controlado (un laboratorio), para observar directamente la degradación de la hojarasca de 
Rhizophora mangle, a través de Xenylla pseudomaritima, y diferentes gremios de ácaros 
(Oribatida y Mesostigmata), encontrando que la mayor degradación de materia es llevada a 
cabo por el colémbolo, los oribátidos y a interacción de ambos, sin embargo la relación de 
competidores, entre estos dos grupos, no se observó. 
En el caso de la relación X. pseudomaritima- mesostigmata, el colémbolo termina por 
desaparecer en el microcosmos a causa del depredador. 
2 
 
Abstract 
Collembola and Oribatida are two important groups arthropods that form the soil mesofauna, 
whose communities are studied in forests and jungles; however, in the mangroves, are poorly 
studied, mainly in Mexico, where the arthropod fauna is unknown, especially in the islands 
Mexican. 
Mexico has a vast territory and rich biodiversity, with large extensions of mangrove 
areas throughout the country, these areas have differences ranging from the vegetation that 
composes until geomorphology. 
In Cozumel, particularly Punta south park can find a vegetation dominated by 
Rhizophora mangle and Avicennia nitida, these trees are found around different lagoons, 
which are only flooded in the rainy season, in addition to being far from the sea are considered 
a mangrove dry. 
Before this study, arthropods of soil mesofauna integrating Cozumel mangroves were 
unknown. Presently we have record of 30 orders, being Oribatida and Collembola more 
abundant. 
Considering only the Collembola, 53 taxa were recorded, being Lepidocyrtus ca. 
floridensis, Hemisotoma thermophila and Xenylla yucatana, the most densely populated; 
similarly a marked seasonal and temperature effect on the structure of Collembola 
community, mainly in the mangroves of Laguna Colombia also a replacement of the 
mangrove studied. 
Furthermore, there has been the importance of processes mesofaunal degradation and 
fragmentation of the litter, plus influence the activity of fungi and bacteria, those are fed; so 
that a study was conducted in a controlled environment (laboratory), to observe directly the 
degradation of litter from Rhizophora mangle through Xenylla pseudomaritima, the guild of 
Oribatida, finding that the further degradation is carried conducted by springtails, oribatid 
and interaction of both. However the ecological competitive relationship between these two 
groups was not observed. 
In the case of predator-prey relationship, mesostigmata- X. pseudomaritima, the springtail 
eventually disappears in microcosm because the predator. 
3 
 
1. Introducción general 
Los colémbolos son un grupo muy importante de hexápodos, que junto con los ácaros, 
constituyen un componente esencial de la mesofauna del suelo. Se encuentran, en casi todos 
los ecosistemas, desde zonas altamente húmedas, hasta las desérticas, excepto mares 
profundos; los encontramos desde el ártico, a la tundra alpina, pasando por los desiertos 
llegando a selvas tropicales y litorales. 
Su densidad puede ser muy alta, teniendo varios millones de individuos por m2, y su 
riqueza varía de 1-3 a más de 60 especies, dependiendo el ecosistema, aunque en muchos de 
ellos, como en el caso de manglares, se desconoce la riqueza que se pueda encontrar (Rusek 
1998). 
Dentro de su estudio, se han realizado diversos trabajos, enfocados ya sea sobre su 
importancia ecológica o taxonómica, así como en su función en el suelo, como componentes 
de la comunidad de la mesofauna, o por sus hábitos alimenticios; de igual forma se han 
realizado trabajos sobre el papel que desempeñan estos organismos en la formación del suelo; 
sin embargo, en los diferentes estudios sobre los litorales, no se ha visto el papel que 
desempeñan en la formación y mantenimiento de dicho sustrato. 
 
1.1 Collembola 
Los colémbolos son pequeños animales que van desde micrones (Megalothorax) hasta casi 
los dos centímetro de largo (Holocanthella). Estos artrópodos sin alas, similares a los 
insectos, se dividen en cuatro Órdenes: Poduromorpha, Entomobryomorpha, Symphypleona 
y Neelipleona (Bellinger, et al. 2015). Los dos primeros presentan un cuerpo más o menos 
alargado y los restantes lo tienen de forma globosa. 
La estructura que le dá el nombre, es el tubo ventral o colóforo, el cual consiste en un 
saco eversible en el primer segmento abdominal (Chistiansen 1992). Dicho órgano es 
extremadamente importante para el balance de fluidos, y puede ser usado como un apéndice 
pegajoso, el cual les permite adherirse a superficies resbalosas (Hopkin 2002), u hojarasca, 
que en el caso de los litorales marinos, se encuentra flotando. 
Los colémbolos se distribuyen globalmente, siendo abundantes en todos los continentes, 
incluyendo la Antártida, donde se ha encontrado a las especies Biscoia sudpolaris y 
Antarctophorus subpolaris sobre líquenes. Además es frecuente encontrarlos a la orilla del 
4 
 
mar, como es el caso de Anurida maritima, una especie común de los litorales europeos 
(Hopkin 1997), o Archisotoma megalops, cuya abundancia fue de 3 200 organismos, en la 
playa de Spitsbergen, Noruega (Leinaas y Ambrose 1992). 
Por otro lado, números estudios muestran que la mayoría de los colémbolos habitan tanto 
en la hojarasca, como en el humus (Larsen, et al. 2003), por lo que juegan un papel importante 
en la microestructura del suelo, representando una fracción cualitativa y cuantitativamente 
muy importante de la fauna edáfica. Así, la biomasa del grupo aumenta conforme las 
condiciones ambientales se tornan más estables y húmedas, por ejemplo, se ha estimado en 
150 mg de masa seca por m2 en la tundra y de 20 mg en un bosque tropical (Rusek 1998); 
sin embargo, en los diferentes suelos que se encuentran en los litorales marinos, no se ha 
estimado su biomasa. 
Rusek (1998), mencionó que los colémbolos son generalmente micófagos, es decir, no 
digieren la celulosa ni la lignina, pero se alimentan de micelios, donde los elementos ya se 
encuentran transformados. Además, estos artrópodos sólo se alimentan de los organismos 
senescentes (Tissaux 1996). La acción de los colémbolos es tan fuerte sobre las diferentes 
poblaciones fúngicas, que pueden llegar a afectar la estructura de las comunidades de hongos 
en el reciclaje de nutrientes (Parkinson, et al. 1979). 
Por otro lado, los cambios físicos del suelo afectan directamente a las comunidades, ya 
sea positiva o negativamente, por ejemplo, las poblaciones pueden disminuir conforme 
aumenta la depositación de los diferentes ácidos o de la lignina (Rusek y Marshall 2000), o 
simplemente del aumento o disminución del pH (Cutz-Pool 2003). 
 
1.2 Adaptaciones de Collembola al medio litoral 
Algunos autores, mencionan que los colémbolos presentan adaptaciones ante el medio litoral; 
por ejemplo, en Parisotoma octooculata, Onychiurus arcticus y Cryptopygus antarcticus, 
mostraron un aumento en la tasa respiratoria, con relación a la temperatura y la humedad, en 
estos ambientes (acuáticos), lo que sugiere que existe un adelgazamiento de la cutícula para 
realizar eficazmente el intercambio gaseoso (Block 1994, Burn 1984). 
Por otro lado, en los manglares se ha observado un sustrato pobre y en continua erosión, 
donde la cantidad de hojarasca tiende a escasear debido a los fuertes vientos y a las mareas 
5 
 
(López y Escurra 2002), así mismo se ha observado una migración vertical, por parte de los 
colémbolos, principalmente en la época de secas, ocultándose en el mantillo (Burn 1984). 
Con referencia a la regulación osmótica, algunos colémbolos de los litorales muestran 
diferencias en su cutícula al tener una mayor cantidad de glándulas (Jordana 1997), éstas 
probablemente actúan para la regulación hídrica al igual que el colóforo al retener o expeler 
sales, dependiendo del sitiodonde se encuentre. Sin embargo, mediante este proceso se puede 
perder agua debido a las condiciones hiperosmóticas presentes en el medio acuoso. A pesar 
de ello, Anurida maritima y Archisotoma pulchella, especies terrestres adaptadas 
fisiológicamente a ambientes salinos, han modificado la concentración osmótica de su 
hemolinfa, presentando solutos orgánicos que, en concentraciones altas de salinidad, pueden 
mantener el equilibrio con el ambiente externo y presentar una concentración baja de iones 
(Witteveen, et al. 1987). 
Las diferentes estrategias que tienen los colémbolos, les permiten sobrevivir en los 
litorales, tanto por las fluctuaciones de temperatura que se tienen en las diferentes épocas del 
año, así como por los constantes cambios, de temperatura y humedad (en cortos periodos de 
tiempo), que se presentan en los suelos (Beard, et al. 2005). Entre sus estrategias se encuentra 
el ciclo de vida; éste es corto en especies tropicales y, generalmente, existe una disminución 
de las poblaciones que se encuentran en las hojarascas del litoral. En las dunas las especies 
mantienen sus poblaciones como ocurre en Folsomia candida (Fountain y Hopkin 2005). 
Cabe señalar que las especies tropicales son univoltinas, y las adaptadas a climas fríos son 
bivoltinas tal es el caso de Parisotoma octooculata (Burn 1984). 
 
1.3 Ecosistema tropical 
A lo largo de la línea costera podemos observar diferentes tipos de vegetación, como selvas, 
manglares, selvas y riveras (Lugo & Snedaker 1974); de estos, los manglares representan 
aproximadamente 181, 000 km2 (Twilley et al. 1996), localizándose en la zona intermareal 
de ríos, deltas, lagos, lagunas y estuarios de las costas; colonizando las orillas de las 
plataformas calcáreas (Woodroffe 1990). 
En México, el manglar se distribuyen en el interior de lagunas costeras y sistemas 
deltaicos de las costas del Golfo de México y del Océano Pacífico, con una distribución de 
Baja California y Sonora, hasta Chiapas (Carranza et al. 1975); y del lado del Golfo de 
6 
 
México (de localidades de mayor humedad) se localizan generalmente en zonas protegidas, 
que presentan escorrentía continental, iniciando en Tamaulipas pasando por las costas del 
Golfo hasta llegar al Mar Caribe (López-Portillo y Ezcurra 2002). 
En el caso de la península de Yucatán, el manglar es enano (1.5-2 m), derivado del 
paisaje de carso, así como la influencia saturada de calcio, la pobreza de los nutrientes 
(López-Portillo y Ezcurra 2002), la salinidad (Ball y Farquhar 1984), el nivel de inundación 
y los niveles de marea (Adams 1963), siendo las islas caribeñas donde mejor se puede 
observar esta fisionomía, como se muestra en la Isla de Cozumel, donde se encuentran 
pequeños bosques compuestos por Rhizophora mangle o Avicennia nitida (nunca 
combinados) a las orillas de las lagunas, sin tener contacto directo con las marismas del Golfo 
de México. 
En lo referente a la Península de Yucatán, se han realizado estudios sobre la producción 
de hojarasca en R. mangle y la alta salinidad en Laguna de Términos, Campeche (Day Jr. et 
al. 1987), así como la estructura de la vegetación en los manglares (Trejo-Torres et al. 1993) 
y el efecto de los huracanes sobre este ecosistema (Whigham et al. 1991). 
Para el 2009 se publicó el libro: “El sistema ecológico de la bahía de Chetumal/Corozal: 
costa occidental del Mar del Caribe”, en él se habla sobre la hidrología de la cuenca del 
Caribe, además de aspectos bióticos y abióticos del sitio, así como de la fauna existente en la 
bahía; sin embargo, no se abordan temas sobre degradación, descomposición o producción 
de biomasa de hojarasca en este sistema acuático (Espinoza-Ávalos et al. 2009). 
 
1.4 Collembola y el medio litoral 
La fauna edáfica, de los litorales, ha sido poco estudiada, principalmente en lo referente a 
colémbolos; sin embargo, se ha registrado que, junto a Oribatida, llegan a representar hasta 
el 97% de la densidad de organismos, siendo los Collembola el segundo grupo más abundante 
(Netto y Gallucc, 2003). 
Con relación a su diversidad, se han colectado 186 especies en litorales, y arenas (dunas), 
presentando un endemismo del 45% y un 12% cosmopolita. Los géneros más comunes, de 
colémbolos, que se han encontrado son: Willemia, Xenyllogastrura, Axenyllodes, Friesea, 
Micranurida, Doutnacia, Mesaphorura, Onychiurus, Protaphorura, Scaphaphorura, 
7 
 
Tullbergia, Isotogastrura, Archistosoma, Folsomia, Folsomides, Folsomina e Isotomodes 
(Thibaud 2007). 
Por otro lado, y aunado a la distribución de especies cosmopolitas, se concluyó que son 
organismos subacuáticos (Coulson et al. 2000), ya que en ciertos experimentos fueron 
expuestos a la película superficial de agua sobreviviendo 14 días, y Tetracanthella arctica, 
sobrevivió inmersa en el mar hasta dos semanas (Thibaud 2007), concluyendo que la 
dispersión y colonización hacia otros litorales puede ser dada a través de los océanos. 
 
1.5 Degradación de la materia orgánica 
En el proceso de la degradación de la materia orgánica, se presentan tres fases básicas, en las 
que influye la constitución de los materiales que se degradan (manglares, pastos). Estas fases 
referidas involucran la lixiviación de los componentes solubles, la oxidación microbiana y la 
fragmentación física, así como biológica, que efectúan la meso y macrofauna (Valiela et al. 
1985). 
Con bolsas para medir la degradación de hojarasca en manglares, se observó una pérdida 
de peso de hasta un 40% del sustrato, entre 35 a 40 días, dada por el clima y sin la presencia 
de meso y macro fauna, además se observó que el nitrógeno (N) disminuye, ocasionando una 
lenta colonización de invertebrados fragmentadores y descomponedores, pero una vez que se 
han iniciado el establecimiento de la mesofauna, pueden modificar el ambiente físico y 
químico del mantillo, aumentando las concentraciones de N (al inmovilizarlo), y el arresto 
del carbono (Wang y Ruan 2011), dando por resultado un incremento de la fauna, 
principalmente de colémbolos. 
Entre los grupos, que facilitan y modifican el medio, se encuentran los colémbolos, 
quienes se alimentan de micorrizas, hongos saprófitos y aceleran la transferencia de 
nutrientes entre el mantillo, el suelo mineral y las raíces de plantas; además su tamaño 
pequeño les permite aumentar su distribución entre los espacios que se encuentran entre la 
hojarasca de forma más eficiente, así como incrementan la cantidad de agregados (Brand y 
Dunn 1998). 
La acción de los hongos es importante, ya que, se ha registrado una mayor diversidad y 
abundancia de éstos, en los manglares, con relación a las bacterias (Coleman et al. 2004). 
 
8 
 
1.6 Colémbolos y degradación de la materia orgánica del suelo 
Es posible que existan más de 100 especies de Collembola en los litorales, pero en las 
investigaciones que se han realizado, sólo se presentan como grupo funcional, sin mostrar 
interés por las especies que están involucradas en dicho proceso (Hossain y Fazlul 2008). En 
otros casos, sólo llevan a cabo listado de especies o grupo de organismos que se encuentran 
en estos sitios (Thibaud y Palacios-Vargas 2000), como son: Isogastrura ahuizotli, I. 
atuberculata, I. veracruzana, I. arenicola, I. coronata, I, madagascariensis, I, trichaetosa, I. 
litoralis (Potatov et al. 2011), Folsomia candida, Pseudachorutes cf. parvulus, Mesaphorura 
yosiii, Folsomides parvulus y F. onychiurina (Bandyopadhyaya y Kumar 2000). 
En otros trabajos se han realizado estudios sobre el contenido estomacal de algunas 
especies de Collembola de litorales, donde se hallaron restos de diatomeas, así como detritos 
de pastos y mangles (Mertens et al, 2007), haciéndolos importantes en el inicio de las cadenas 
tróficas y de la formación de suelos. 
Dentro de la formación de la paedogénesis, los colémbolos cumplen diferentes 
actividades, principalmente como fragmentan hojarasca y dispersanbacterias y hongos y de 
esta forma incrementan el área de colonización y descomposición microbiana. Además se 
encuentran los micropelets, importantes en el reciclaje de nitrógeno (Showalter, 2006), 
además de facilitar la formación de nuevos suelos (Coleman et al. 2004). 
 
 
 
 
 
 
 
 
 
 
 
 
 
9 
 
2. Justificación 
Los colémbolos, forman parte del gremio de microartrópodos que se alimentan 
principalmente de hongos y bacterias, siendo los principales organismos que se encargan de 
degradar la hojarasca del mantillo en suelos de bosques templaos y selvas. Sin embargo, en 
los litorales, particularmente los manglares, se ha observado que la degradación se lleva a 
cabo principalmente por hongos, bacterias y algas. 
Por otro lado, la mesofauna asociada en estos bosques, en su mayoría es poco conocida, 
así como sus interacciones ecológicas inter e intraespecífica. Así mismo se desconoce la 
descomposición de hojarasca a través de la acción de colémbolos y ácaros. 
De ahí la importancia de conocer las comunidades de colémbolos asociados a manglares 
secos enanos de la Isla de Cozumel, México. Ya que nos permitiría saber, la época del año 
en que dichas comunidades llevan a cabo la mayor tasa de degradación de hojarasca, 
permitiendo que los nutrientes se reincorporen a otros sistemas, por ejemplo los corales. 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
10 
 
3. Resumen de capítulos 
Para el desarrollo de la investigación del papel de los colémbolos en los procesos de 
degradación de hojarasca en los manglares de la Isla de Cozumel, México, se abordaron dos 
subtemas, los cuales se dividieron en tres capítulos. 
 
Capítulo I 
Mesofaunal arthropod diversity in shrub mangrove litter of Cozumel Islan, Quintana 
Roo, México 
(Publicado) 
Se refiere sobre la distribución y diversidad de las comunidades de artrópodos de los 
manglares del Parque Punta Sur de Cozumel, encontrando que los factores de temperatura y 
temporalidad son importantes para el establecimiento y abundancia de los 30 órdenes y 
subórdenes de artrópodos, siendo Oribatida y Collembola los taxones de mayor 
representatividad a lo largo de un año (noviembre 2011 a marzo del 2012). 
 
Capítulo II 
Diversity and distribution of Collembola (Hexapoda) in two mangroves, in Punta Sur, 
Cozumel, Mexico 
(En revisión) 
Se refiere sobre la distribución y diversidad de las comunidades de colémbolos de los 
manglares del Parque Punta Sur de Cozumel. Se colectaron 13,673 organismos, divididos en 
53 especies, siendo Lepidocyrtus ca. floridensis, Hemisotoma thermophila y Xenylla 
yucatana, las especies de mayor abundancia, de igual forma se observó un marcado efecto 
estacional sobre la estructura de las comunidad de Collembola, además se registró un 
recambio de especies entre los manglares estudiados (Rhizophora mangle y Avicennia 
nitida). 
 
Capítulo III 
Cambios en la degradación de hojarasca de Rhizophora mangle L. bajo diferentes 
tipos de interacciones de Xenylla pseudomaritima 
 (En preparación) 
11 
 
Se refiere, al trabajo en laboratorio sobre el proceso de degradación de hojarasca de 
Rhizophora mangle, a través de Xenylla pseudomaritima, además de las interacciones 
ecológicas de competencia, con el gremio de oribátidos, y depredación con mesostigmados; 
estos resultados nos mostraron que en comunidades de microartrópodos la competencia no 
existe, sino que los diferentes grupos que interactúan sólo coexisten en el microcosmos del 
diseño experimental. 
 
Applied Soil Ecology 83 (2014) 44–50
Contents lists available at ScienceDirect
Applied Soil Ecology
jo u r n al homep ag e: www.elsev ier .com/ locate /apsoi l
Mesofaunal arthropod diversity in shrub mangrove litter of Cozumel
Island, Quintana Roo, México
Arturo García-Gómez a, Gabriela Castaño-Meneses a,b,∗,
M. Magdalena Vázquez-González c, José G. Palacios-Vargas a
a Ecología y Sistemática de Microartrópodos, Depto. de Ecología y Recursos Naturales, Fac. Ciencias, Universidad Nacional Autónoma de México,
Coyoacán 04510, México, D.F., Mexico
b Unidad Multidisciplinaria de Docencia e Investigación, Fac. Ciencias, Campus Juriquilla, UNAM, Juriquilla 76230, Querétaro, Mexico
c Departamento de Ciencias, División de Ciencias e Ingeniería, Universidad de Quintana Roo, Quintana Roo, Mexico
a r t i c l e i n f o
Article history:
Received 24 January 2013
Received in revised form 15 March 2014
Accepted 17 March 2014
Available online 29 April 2014
Keywords:
Community
Soil
Oribatida
Collembola
a b s t r a c t
We studied the mesofaunal arthropod diversity in a shrub mangrove in the Punta Sur area within the
National Park Reefs of Cozumel Island in the South of Mexico. Two mangrove areas were selected for
sampling, dominated by Rhizophora mangle and Avicennia nitida, respectively. Four sampling periods, two
during the dry season and two during the rainy season, and 25 random litter samples of litter (225 cm2)
per site and date led to a total of 200 samples. Spatial and temporal variation of arthropod diversity was
analyzed at the order/suborder level. A total of 90,680 arthropods belonging to 30 taxa were recorded
during the study, Oribatida being most abundant with 61.8%, followed by springtails (14%). Densities of
arthropods were higher in the rainy season than in the dry season, showing a strong positive correlation
with humidity. Highest abundance was found in the R. mangle mangrove in the rainy season, and highest
diversity was found in the A. nitida mangrove in the dry season. Seasonal distribution of litter fauna in
two mangroves are related with the particular characteristics shown in each one.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Mangroves are ecosystems at the transition from the terrestrial
to the marine habitat, characterized by strong spatial and temporal
variations of factors such as inundation, salinity, temperature and
oxygen. Compared to other environments, for example rain forests,
mangroves show high productivity and low species richness (Duke
et al., 1998), the latter because of the extreme fluctuations of envi-
ronmental factors that require special adaptations of the species
(Field et al., 1998; Whittaker et al., 2001). Only few plant families,
e.g. Rhizophoraceae, Avicenniaceae and Combretaceae have devel-
oped physiological and structural adaptations, comprising about
50–70 species only, depending on different classifications (FAO,
2007). These trees are used as refuge for fungi (Kathiresan and
Bingham, 2001), bacteria (Twilley et al., 1996), plants and animals
∗ Corresponding author at: Ecología y Sistemática de Microartrópodos, Depto. de
Ecología y Recursos Naturales, Fac. Ciencias, Universidad Nacional Autónoma de
México, Coyoacán 04510, México, D.F., Mexico. Tel.: +52 55 56 22 49 02;
fax: +52 55 56 22 48 28.
E-mail addresses: gabycast99@hotmail.com, gabrielacatano@yahoo.com.mx
(G. Castaño-Meneses).
(Meades et al., 2002) with terrestrial, aquatic and/or semiaquatic
habits. Fauna and flora in the mangroves are organized in complex
trophic webs with interactions among aquatic (fishes), terrestrial
(birds, mammals, reptiles, arthropods; Nagelkerken et al., 2008),
and amphibiotic biota (crabs; Smith et al., 1991; insects, Moreno-
Casasola and Infante, 2009; amphibians, reptiles; Nagelkerken
et al., 2008; mollusks; Kathiresan and Bingham, 2001). Further-
more, the temporal and spatial variations of environmental factors
are reflected in the temporal and spatial distribution of species, as
it has been documented in ants of mangroves (Nielsen, 2011).
Throughout the world, about 10,000–240,000 km2 of the trop-
ical and subtropical littoral belt are mangroves (Moreno-Casasola
and Infante, 2009; Giri et al., 2011), but these ecosystemsare seri-
ously endangered. In Mexico, according to data from 2008, there
are 655,667 ha of mangroves, 55% of them located in the Yucatán
Peninsula, and 16% alone in Quintana Roo State (Comisión Nacional
de Biodiversidad, CONABIO, 2009). Here ca. 20% of this ecosystem
have been destroyed in only 15 years, from 1986 to 2001, due to
human population growth and the increase of tourism industry, ca.
20% of this ecosystem has been destroyed in Quintana Roo State
in only 15 years, from 1986 to 2001 (Moreno-Casasola and Infante,
2009). The area has recently been recognized as a priority for con-
servation by the CONABIO, the Mexican National Commission of
http://dx.doi.org/10.1016/j.apsoil.2014.03.013
0929-1393/© 2014 Elsevier B.V. All rights reserved.
A. García-Gómez et al. / Applied Soil Ecology 83 (2014) 44–50 45
Fig. 1. Localization of studied lagoons at Punta Sur Park, Cozumel, México.
Biodiversity (CONABIO, 2009), nevertheless mangroves continue
to be affected and reduced, even in protected areas such as Punta
Sur, Cozumel.
Most studies on mesofauna of mangroves have focused on
groups such as ants, larvae of dipterans and beetles (Twilley et al.,
1996), copepods, mites, termites and springtails (Procheş et al.,
2001; Nagelkerken et al., 2008). Very few ecological studies in Mex-
ican mangroves are available (Dejean et al., 2003). The Quintana Roo
mangroves in Chetumal have been investigated regarding physical
and environmental aspects, a and b diversity of biota, and envi-
ronmental protection (Espinoza-Ávalos et al., 2009), descriptions
of new species of springtails (Thibaud and Palacios-Vargas, 2001),
new records of springtails (Cutz-Pool and Vázquez-González,
2012), and records of ants and termites (Moreno-Casasola and
Infante, 2009). Currently 28 species of springtails are known from
mangroves in Cozumel (Cutz-Pool and Vázquez-González, 2012).
In the present study we analyze the seasonal and spatial vari-
ations in diversity of invertebrates in litter of mangroves from
Cozumel Island. We compared two areas with different species
of mangrove, one characterized by Rhizophora mangle (red man-
grove) as the dominant trees species, the other characterized by
Avicennia nitida, a species that on Cozumel Island replaces Avicen-
nia germinans (black mangrove), usually present in Quintana Roo
(Moreno-Casasola and Infante, 2009). Being a preliminary study
we considered higher taxa levels. Studies focusing on conservation
suggest that the higher taxon approach can be applied for conser-
vation purposes in order to predict species richness (Gaston and
Williams, 1993).
2. Materials and methods
2.1. Study area
Cozumel Island (20◦30′N and 86◦57′W) is located at the North-
east of the Yucatán Peninsula. We studied two lagoons (Fig. 1)
at the South of the Island, in the Punta Sur Ecological Park. The
Colombia Lagoon (20◦18.27′43′′N, 87◦00.43′47′′W) to the east is
dominated by Rhizhopora mangle L.; the Chun Chacaab Lagoon to
Table 1
Characteristics between lagoons from Punta Sur, Cozumel.
Colombia Lagoon Chuc Chacaab
Lagoon
Localization 20◦18.27′43′′N,
87◦00.43′47′′W
20◦18.01′47′′N,
87◦00.39′71′′W
Dominant tree Rhizophora mangle Avicennia nitida
Distance to the sea 20–25 m 45–50 m
Altitude 0.5–2.5 2–4
Dunes Without Several more than
to 10 m high
the west (20◦18.01′47′′N, 87◦00.39′71′′W) is dominated by A. nitida
Jacq. (Arriaga et al., 2000).
The area is colonized by dwarf mangrove (Moreno-Casasola and
Infante, 2009). The limited growth of the mangrove trees is possi-
bly due to the karstic bedrock which leads to low exchange rates
of the water body (in terms of tidal influence and fresh water
input) and produces calcium saturated water with few nutrients
and shallow soils (López and Ezcurra, 2002). Each lagoon has par-
ticular characteristics, shown in Table 1. During the rainy season
(June–December), both lagoons are connected; there are frequent
hurricanes in the area with strong winds. In the dry season (January
to May), Colombia Lagoon shows little influence of wave motion
and the area is almost dry, while Chun Chacaab Lagoon shows a
natural opening (between dunes) where the ocean water comes
in and preserves the humidity in the area during the dry months.
There is no sand in both lagoons, dunes in the East area excepted,
and roots and pneumatophores of mangroves are on karstic rocks;
only in the rainy season there is stagnant water. The dunes are a
natural barrier to the entrance of marine water. The tidal range in
the area is considered microtidal with a typical range of less than
20 cm (Kjerfve, 1981). There are no data about the pH in the studied
area, but in wells of the urban zone of Cozumel, levels ranged from
7.5 to 8.7 (Coronado-Álvarez et al., 2011). Merino and Otero (1983)
reported salinities at Puerto Morelos in the range of 36.8–32.3‰.
2.2. Sampling
Four expeditions were performed to Cozumel Island, in April,
September and November 2011 and in March 2012. In each lagoon
we selected five sites, and five samples of litter were taken per
site. Each sampled surface was 225 cm2. The depth of litter was
about 2 cm in the area, accumulated between pneumatophores
and the soil surface. Litter samples were stored in plastic boxes
10.5 cm × 10.5 cm × 5 cm (551 cm3). Sampling points were selected
in one transect of 20 m, and by random number sampling points
were obtained. A total of 25 samples were taken in each lagoon
on each occasion, resulting in a total of 200 samples for the whole
study. Data of temperature, relative humidity and CO2 content were
taken in each sampling point using a multimeter (IAQ-CALC 8760-
M-NP).
Samples were carried to the Laboratorio de Ecología y Sis-
temática de Microartrópodos at Science Faculty, UNAM, and
processed by Berlese funnels during six days, first three with nat-
ural light and the last three with a heat source (60 W bulb). The
fauna obtained was fixed in 75% ethanol, counted and identified
to the order and suborder level using a stereo-microscope. Speci-
mens were identified to morphospecies level, however, the analysis
presented here confines to order/suborder level. Further results
concerning the species level will be presented elsewhere.
2.3. Statistical analyses
Shannon diversity index was calculated for site and samp-
ling data, and comparisons were made by “t” student test and
46 A. García-Gómez et al. / Applied Soil Ecology 83 (2014) 44–50
Table 2
Abundance recorded by taxa in mangroves of Cozumel Island. I = Rhizophora mangle. II = Avicennia nitida. S = Species richness, H′ = Shannon’s diversity index, J′ = Pielou’s
evenness index and � = Simpson dominance.
Taxa April 2011 September 2011 November 2011 March 2012 Total
I II I II I II I II I II
Amphipoda 0 0 0 1 1 9 0 0 1 10
Isopoda 8 4 91 31 46 79 1 54 146 168
Chilopoda 0 1 36 19 4 6 2 8 42 34
Diplopoda 0 0 22 33 34 10 9 25 65 68
Symphyla 0 0 21 7 15 0 0 1 36 8
Araneae 22 98 101 91 120 119 56 60 299 368
Scorpionida 0 0 0 0 0 0 1 0 1 0
Solifuga 0 0 0 0 0 0 0 1 0 1
Pseudoscorpionida 7 1 63 47 45 50 21 57 136 155
Opilionida 0 0 0 0 1 0 0 0 1 0
Opiliocarida 0 0 5 0 12 1 5 0 22 1
Mesostigmata 92 380 3 732 3 703 2 167 1 404 154 603 6 145 6 090
Oribatida 221 1385 18 606 13 142 6 821 10 227 930 4 689 26 578 29 443
Prostigmata 152 531 440 928 452 407 380 1 015 1 424 2 881
Protura 0 0 57 18 18 0 0 0 75 18
Diplura 0 0 9 3 5 0 0 0 14 3
Collembola 8 12 6044 3 727 1 894 753 10 210 7 956 4 702
Zygentoma 0 2 5 20 3 5 17 13 25 40
Orthoptera 1 9 1 5 6 20 6 5 14 39
Blattodea 4 7 4 3 40 38 8 7 56 55
Isoptera 0 0 0 0 11 0 0 13 11 13
Embioptera 0 0 6 1 1 0 1 6 8 7
Thysanoptera 132 44 53 107 123 331 69 250 377 732
Psocoptera 48 288 197 88 59 29 109 256 413 661
Heteroptera 2 6 9 15 6 13 1 5 18 39
Homoptera 14 9 310 79 26 980 59 430 156
Neuroptera 0 0 2 0 1 0 0 0 3 0
Coleoptera 105 14 24 25 38 22 14 81 181 142
Hymenoptera 3 11 28 55 72 56 12 8 115 130
Diptera 81 6 10 9 6 6 2 3 99 24
Lepidoptera 0 0 0 0 0 1 0 0 0 1
Total 900 2 808 29 876 22 157 12 027 13 595 1 888 7 429 44 691 45 989
Density ind/m2 20 63 672 499 271 306 42 167 1 006 1 035
S 16 18 25 24 28 22 22 23 29 28
H′ 2.12 1.51 1.13 1.22 1.35 1 1.70 1.38 1.31 1.27
J′ 0.76 0.52 0.35 0.38 0.40 0.32 0.55 0.44 0.40 0.44
� 0.14 0.30 0.44 0.40 0.38 0.58 0.29 0.42 0.39 0.38
Total density 83 1 171 25 622 9 317 2 041
Bonferroni correction ( ̨ = 0.004) for multiple comparisons (Zar,
1984; Magurran, 1988). Pielou’s evenness and Simpson dominance
were calculated as well. The analyses were performed in STATECOL
ver. 1.12 software.
The effect of the mangrove tree species (R. mangle and A. nitida)
and sampling date (four times) on the mesofauna abundance was
evaluated by a factorial analysis of variance (ANOVA), the differ-
ences were tested by post hoc Tukey’s test. Relationships between
environmental parameters (temperature, relative humidity and
CO2 concentration), and fauna abundance was evaluated by mul-
tiple correlations. Data were transformed by
√
x + 0.5 in order to
normalized their distribution (Zar, 1984). Analyses were performed
in STATISTICA ver.8.0 software (StatSoft Inc, 2007).
3. Results
3.1. Abundance and arthropod diversity
During the study a total of 90,680 arthropods belonging to 30
order and suborder taxa were collected. Most abundant was Orib-
atida with 61.8% of all arthropods collected, followed by Collembola
(14%) and Mesostigmata (13.5%). The remaining taxa were below
5% abundance (Fig. 2), and included crustaceans (Amphipoda
and Isopoda), myriapods (Chilopoda, Diplopoda and Symphyla),
arachnids (Scorpionida, Solifugae, Araneae, Pseudoscorpionida,
Opilionida, Opilioacarida and Prostigmata) and hexapods (Protura,
Diplura, Zygentoma, Orthoptera, Blattodea, Isoptera, Embioptera,
Thysanoptera, Psocoptera, Hemiptera, Neuroptera, Coleoptera,
Hymenoptera, Diptera and Lepidoptera).
In A. nitida mangroves (Chun Chacaab Lagoon) 45,989 speci-
mens were collected, and in R. mangle mangrove (Colombia Lagoon)
44,691 specimens. At the former site Oribatida and Prostigmata
were the most abundant arthropods, and at the latter Collembola
and Mesostigmata (Table 2). Thysanoptera and Psocoptera were
the most abundant insects at both sites, with more than 1000 spec-
imens collected (Table 2). In the case of arachnids (excluding mites),
spiders were most abundant (667 specimens); among myriapods,
Fig. 2. Percentages of mesofaunal arthropods collected in litter from two mangroves
at Punta Sur, Cozumel, México.
A. García-Gómez et al. / Applied Soil Ecology 83 (2014) 44–50 47
Table 3
Density (±sd) of the two most abundant groups registered in two mangroves at Punta Sur Ecological Park.
April 2011 September 2011 November 2011 March 02012 Total
Oribatida 36 ± 0.13 714 ± 1.7838 384 ± 0.9132 127 ± 0.4417 1260 ± 3.2
Collembola 1a ± 0.0025 220 ± 0.6878 60 ± 0.2766 5 ± 0.0607 285 ± 1.02
a Density < 1 ind m−1 .
most abundant were millipedes (133), and among crustaceans,
isopods (168).
Highest abundances at both sites were recorded during the rainy
season (September and November) and lowest abundances during
the driest months (March and April). The highest values of diversity
and evenness were recorded in the R. mangle mangrove (Table 2),
however, no significant differences were found between diversity
indices of the two lagoons (t test, t0.06, 199 = 0.19, p > 0.05). Regarding
temporal variation, in both sites highest values in diversity and
evenness indices were found in April, while the lowest values in
diversity corresponded to September; as for evenness, the lowest
value was found in November (Table 2). Significant differences were
found in the diversity indices between April and September (t0.06,
199 = 3.6, p < 0.05) and between April and November (t0.06, 193 = 3.3,
p < 0.05).
In the R. mangle mangrove, diversity and evenness of arthropods
showed the same temporal pattern (Table 2), with significant differ-
ences between April and September (t0.06, 199 = 7.02, p < 0.05), April
and November (t0.06, 197 = 5.16, p < 0.05), and between September
and March (t0.06, 198 = −3.27, p < 0.05). In the A. nitida mangrove, on
the other hand, the highest values in diversity and evenness were
recorded in March and the lowest in September, but no significant
differences were found (t0.06, 198 = 0.08, p > 0.05).
Mean total mesofaunal arthropod density at both sites was
2040 ind/m2, with highest values found during the rainy season
and the lowest in April (Table 2).
Many groups of arthropods were represented by very few spec-
imens, some by only one specimen (Table 2), for example Solifugae
and Opilioacarida in the A. nitida mangrove. The best represented
groups in density were Oribatida and Collembola, and temporal
variations are shown in Table 3.
3.2. Effect of collection date and habitat on arthropod density
Regarding total arthropod density, ANOVA factorial test results
showed a significant effect of sampling dates and their interaction
with site (Table 4), but the site alone had no significant effect on
density. In the case of the most abundant groups, the same results
were observed in Oribatida, while in Collembola all variables had
a significant effect on their density (Table 4). Tukey’s test showed
significant differences in invertebrate density between April and
March in the R. mangle mangrove, while in the A. nitida mangrove
differences were found between April and the remaining months
(Fig. 3).
In the case of the oribatid mites, the same pattern as in all arthro-
pods was found in the Colombia Lagoon (R. mangle), while in Chun
Chacaab Lagoon (A. nitida) there were differences between den-
sities recorded in April and March and between September and
November (Fig. 4), while for Collembola, significant differences
were found only in the A. nitida mangrove, where September dif-
fered from the other months (Fig. 5).
3.3. Effects of abiotic parameters on arthropod communities
A positive and significant relationship was found between rel-
ative humidity and total arthropod abundance (r40 = 0.5; p < 0.05),
while the temperature was negatively correlated with abundance
(r40 = −0.23, p < 0.05; Fig. 6). No significant correlation was found
Table 4
Factorial analysis of variance (ANOVA), to effect of mangrove species and date of
collection on total arthropods abundance, Oribatida, Mesostigmata and Collembola.
p < 0.05, ns = no significant.
Arthropoda
g. l. F p
Collection date 3 88.64 **
Habitat 1 1.52 ns
Collection date × habitat 3 7.34 **
Oribatida
Collection date 3 60.20 **
Habitat 1 2.77 ns
Collection date × habitat 3 6.92 **
Mesostigmata
Collection date 3 55.9 **
Habitat 1 0.272 ns
Collection date × habitat 3 2.18 ns
Collembola
Collection date 3 68.73 **
Habitat 1 5.46 **
Collection date × habitat 3 3.13 **
for CO2 concentration. Considering Oribatida, the same pattern was
found (Humidity: r37 = 0.56; Temperature: r37 = −0.20, p < 0.05), but
Collembola abundance was positive correlated only with humidity
(r26 = 0.35, p < 0.05)
4. Discussion
Mangroves are very special environments because they are
an ecosystem on the border of two different habitats, terrestrial
and marine, which increase greatly the productivity in compari-
son with temperate and tundra ecosystems (Twilley et al., 1992).
Crustaceans are usually the dominant group in the macrofauna
of mangroves; this includes the community associated with the
pneumatophores, where the arthropod assemblages consist also of
Fig. 3. Factorial ANOVA results of the effect of mangrove type and season on arthro-
pod density at Cozumel, México. ‘=R. mangle.
48 A. García-Gómez et al. /Applied Soil Ecology 83 (2014) 44–50
Fig. 4. Factorial ANOVA results of the effect of mangrove type and season on Orib-
atida density at Cozumel, México. ‘=R. mangle.
mites, and hexapods (mainly collembolans and dipterans), apart
from crustaceans (Procheş et al., 2001). However, in our study
performed in Punta Sur, Cozumel Island, the assemblage of ter-
restrial arthropods in mangroves includes arachnids, myriapods,
crustaceans and hexapods, and the highest density belonged to
mites (mainly Oribatida and Mesostigmata), followed by spring-
tails, a pattern more similar to that in subtropical soils (Sunanda and
Binoy, 2009) and dunes (André et al., 1994) than for a mangrove.
There is little information about soil mesofauna in mangroves
(Karasawa and Hijii, 2004). Regarding pneumatophore communi-
ties, Procheş et al. (2001) found mites that were restricted to this
habitat, prostigmatid mites showed the highest variety of groups
(6 species), while springtails were represented only by Anurida
maritima (Neanuridae). In our study, the oribatid mites were dom-
inant and comprised more than 150 morphospecies, furthermore
30 species of springtails were distinguished (García, unpublished
results). In fact, the habitat is closer to a typically terrestrial habitat
than to a marine one, due to the fact that the pneumatophores are
not covered by water for most of the time, and they are surrounded
by amounts of litter.
The four main groups of arthropods found in our
study—crustaceans, myriapods, arachnids and hexapods—have
Fig. 5. Factorial ANOVA results of the effect of mangrove type and season on Collem-
bola at Cozumel, México. ‘=R. mangle.
Fig. 6. Correlation between arthropod density and environmental parameters: a)
temperature, b) humidity from two mangroves at Punta Sur, Cozumel, Mexico.
also been recorded in other mangroves (Nagelkerken et al.,
2008). Most of the mangroves studied show that crustaceans
and gastropods are the main litter consumers of the macrofaunal
community (Smith et al., 1991; Procheş et al., 2001; Bouillon et al.,
2002). In the studied lagoons of Cozumel Island, due to particular
physical and geological conditions related to the geological history
of the Yucatán Peninsula (Lugo-Hubp et al., 1992), there is no
accumulation of sediment and formation of substrate for the
establishment and development of crustacean and gastropod
populations (A. García, unpublished observation), and the litter
remains longer intact or with fewer traces of fragmentation,
possibly due to the absence of macrofauna. Thus, the mesofauna,
particularly microathropods, is the most important group in the
decomposition process of litter in the area. The few studies that
focused on terrestrial mesofauna of mangroves deal mainly with
morphology and physiology (Friess et al., 2012), some with popula-
tion density of ants (Foster et al., 2011), mosquito larvae (Gwyther
and Fairweather, 2005), and records of beetles, cockroaches,
termites, mites and springtails (Kathiresan and Bingham, 2001).
In Cozumel the same groups were recorded, including others
important in the edaphic environment as myriapods, proturans and
diplurans, as well as some important predators such as scorpions,
pseudoscorpions and solifuges, but in low densities.
In the Colombia Lagoon, dominated by Rizhophora mangle, lower
faunal density values were recorded compared to the Chun Chacaab
A. García-Gómez et al. / Applied Soil Ecology 83 (2014) 44–50 49
Lagoon, probably due to its proximity to the seashore (20–25 m);
the Chun Chacaab Lagoon dominated by A. nitida, is at 50 m from
the sea shore. Temperature and humidity are important parame-
ters in the establishment of communities (Pinto and Swarnamali,
1998). In Cozumel we found that at monthly average temperatures
of ca. 26–28◦ and high humidity, highest densities were recorded,
correlated with the rainy season.
As in similar edaphic environments such as subtropical forests
(Sunanda and Binoy, 2009), mites (mainly Oribatida) and Collem-
bola are the dominant mesofaunal arthropod groups, representing
together between 72 and 97% of all animals extracted.
In both lagoons almost the same number of taxa (order and sub-
order) were found (29 in Colombia Lagoon and 28 in Chun Chacaab
Lagoon). The R. mangle mangrove had highest diversity, whereas
evenness was greater in the A. nitida mangrove, due to the domi-
nance of Oribatida and other groups as Prostigmata, Thysanoptera
and Psocoptera.
The large temporal and spatial variations observed in the study
can be related to the dramatic variations of environmental condi-
tions in these mangroves, due to tidal movements, changing salinity
levels and storms occuring in the area, resulting in an environ-
ment with extreme conditions. Specific adaptations to tolerate such
an environment have been observed in ants (Nielsen, 2011). The
meiofauna associated to pneumatophores shows changes in their
assemblages in relation with salinity, and other studies suggest the
influence of that factor in the composition and distribution of fauna
(Ndaro and Ólafsson, 1999; Procheş et al., 2001). Higher tolerance
towards changes in salinity are required for biota of the Avicennia
mangroves compared to the Rhizopora mangroves (Clough, 1984)
and the fauna associated to the first is adapted to more extreme
conditions in salinity, as has been shown for different groups of
mites (Procheş and Marshall, 2002; Bartsch, 2006). The ability of
different groups to explore the resources in those conditions can
explain the differences in diversity and density of arthropods in
the A. nitida and R. mangle mangroves with higher diversity in the
latter but higher density in the former. Diversity is reduced in the
more stressful environment but species that cope with the environ-
mental conditions can build up larger populations due to reduced
competition and predation.
5. Conclusions
We found a high number of mesofaunal arthropod taxa in our
study, and dominant groups (Oribatida and Collembola) differ from
mangroves studied in other areas, as for example the community
of arthropods associated in pneumatophores.
The highest abundance and richness of taxa was found during
the rainy season, as has been reported in pneumatopore assem-
blages in other mangroves (Procheş et al., 2001; Procheş and
Marshall, 2002), nevertheless, the highest diversity value was
found in April, which is the driest month of the year (Merino and
Otero, 1983).
The mangrove dominated by A. nitida (Chun Chacaab Lagoon)
has shown the highest abundance values, and the dominant group
was Oribatida, while in the R. mangle mangrove (Colombia Lagoon)
Collembola was the dominant group.
Temporal and spatial variations were recorded in the inver-
tebrate communities of both studied mangroves sites. Humidity
affects positively and significantly the abundance of arthropods,
while temperature has a negative effect.
Acknowledgements
The presented research is part of the PhD project of AGG and
the paper constitutes a request to obtain the PhD degree. AGG
acknowledges to Posgrado en Ciencias Biológicas, UNAM, and the
Consejo Nacional de Ciencia y Tecnología (México), for scholar-
ship for his PhD studies. We thank Dr. Rüdiger Schmelz and two
anonymous referees for their valuable suggestions that improved
the manuscript.
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19 
 
Diversity and distribution of Collembola (Hexapoda) in two mangroves in Punta Sur, 
Cozumel, Mexico 
Abstract 
The mesofaunal arthropod diversity was studied in a shrub mangrove in the Punta Sur area, 
within the National Park Reefs of Cozumel Island, in the South of Mexico. Two mangrove 
areas were selected for sampling, dominated by Rhizophora mangle and Avicennia nitida, 
respectively. Four sampling periods, two during the dry season and two during the rainy 
season, and 25 random litter samples of litter (225 cm2) per site and sampling date, for a total 
of 200 samples during the study. Spatial andtemporal variation of Collembola diversity was 
analyzed at specie level. A total of 13,673 springtails belonging to 53 species were recorded 
during the study, Lepidocyrtus ca. floridensis being most abundant representing 15% of total 
abundance, followed by Hemisotoma thermophila and Xenylla yucatana (14%). Densities of 
arthropods were higher in the rainy season than in the dry season, showing a strong positive 
correlation with humidity. Highest abundance was found in the R. mangle mangrove in the 
rainy season, as well as highest diversity. Seasonal distribution of litter fauna in two 
mangroves are related with the particular characteristics shown in each one. 
 
Introduction 
Mangroves are transition ecosystems for terrestrial as well as for aquatic habitats, and are 
defined by diverse and continuous spatial and seasonal variations, as temperature, oxygen, 
floods and strong changes of salinity and pH, due mainly to the action of tides, among other 
factors (Duke et al. 1998). Besides, compared with other environments, as estuaries for 
example, swamps show a high productivity (Flores-Verdugo 1989) and a low vegetal 
richness (Whittaker et al. 2001). 
Mangrove cover between 10 000 and 240 000 km2 of the tropical and subtropical littorals 
around the World (Moreno-Casasola & Infante 2009; Giri et al., 2011). In the case of Mexico, 
approximately 655,667 ha of mangrove area are included, and 55% of them are located in 
the Yucatán Peninsula, from which 16.9% belong to Quintana Roo State. Many ecosystem 
services are offered by mangroves, including the capture of atmospheric carbon, nutrients 
recycling, local weather regulation, and water quality maintenance and flora and fauna 
conservation (CONABIO 2009). 
20 
 
According to the FAO (2007), Rhizophoraceae, Avicenniaceae and Combretaceae 
families present the widest distribution in different mangrove in the World. Those plants have 
developed different physiological and structural adaptations in order to live in these 
environments. It is estimated that these forests are composed by 50 to 70 species, including 
other less numerous, depending on the region where are they development. 
Nevertheless its importance, a high loss of the habitat in this ecosystem has been 
occasioned, mainly by overpopulation and touristic activity in the mentioned areas. As a 
result, in only fifteen years a loss of the 20% of these forest has been recorded (Moreno-
Casasola & Infante 2009). Despite of being priority sites, these areas continue to decrease, 
even in Punta Sur, Cozumel, which, continues to reduce its area due to de forestation. 
In the case of the Cozumel Island, different areas with mangrove are noted, dominated 
by red mangrove (Rhizophora mangle L.) and black mangrove (Avicennia nitida Jacq.) as 
the most representative species (Moreno-Cassasola & Infante 2009). 
In general, the springtails, together with the mites, are essential components of the 
ground mesofauna (Rusek 1998). Their density may be very high, having several millions of 
individuals per m2, and its riches more than 60 species in the same area, depending on the 
type of ecosystem, although in a lot of them, as in the mangrove case and other kind of 
wetlands, the richness that may be found is unknown (Rusek 1998). 
Besides, studies of springtails as part of the fauna in mangrove have been realized 
(Meades et al. 2002). Most of them are taxonomic works (Thibaud & Palacios-Vargas 2001; 
Cutz-Pool & Vázquez-González 2012). In Mexico, particularly Cozumel Island there have 
49 collembolan species records (Cutz-Pool & Vázquez-González 2012), without indications 
if such species are from mangrove or from the rainforest inside the island. 
As it has been mentioned, ecological studies of springtails in mangroves are inexistent, 
particularly at Cozumel Island, which is a conservation area, and has been reduced 
considerably (as well as in all over Mexico). Diversity Collembola in Mexican islands is 
poorly understood. So therefore the structure of the different communities of Collembola in 
two types of mangroves are determined, as well as observing the behavior of the 
colembofauna, to different biotic (vegetation) and abiotoicos factors (temperature, relative 
humidity and porportion of CO2), relative humidity and proportion of CO2) are given 
throughout the year 
21 
 
Material and methods 
Sampling site 
The Cozumel Island (20º 30’ N, 86º 57’ W) is located at the Northeast of the Yucatán 
Peninsula. At the South of the Island two lagoons were studied. In the East of the Punta Sur 
Ecological Park, it is found the Laguna Colombia (20º 18.27’ 43’’ N, 87º 00.43’ 47’’ W) 
where mangrove Rhizophora mangle is the dominant vegetation; and towards at the West it 
is found the Laguna Chuc Chacaab (20º 18.01’ 47’’ N, 87º 00.39’ 71’’ W), dominated by the 
mangrove Avicennia nitida (Arriaga et al. 2000, Fig. 1). 
The mangrove type is called dwarf, because of its limited development (Moreno-
Casasola & Infante 2009), its aspect is due to a hydric active system (it keeps little water), 
besides of the influence of the tides and the entrance of sweet water, along with the karst 
substratum, cause a calcium saturated environment with few nutrients and little deep grounds. 
During the rainy season (June to December), hurricanes and strong winds are frequent 
and causing the connection of both lagoons, and in the dry season (January to May), their 
isolation. 
It must be noted that both mangroves do not show direct influence from the sea; in the 
case of the Laguna Chuc Chacaab, they are far from the sea between 40 and 50 m. Besides 
they present dunes more than 10 m high that prevent the access of the sea, excepting for a 
natural entrance. In the case of the Laguna Colombia, it is between 20 and 25 m far from the 
sea, without any kind of natural barrier, giving as a result the regular introduction of marine 
water. Although it was not observed during our study. 
Another characteristic is the absence of sand, except in the zone of dunes, although the 
amount of sand over them is reduced; nevertheless a big amount of roots and 
pneumatophores are observed. 
 
Sampling 
Four expeditions to island of Cozumel were performed in April, September and November 
of 2011 and March of 2012. In every lagoon five sites were selected, taking five samples of 
dead leaves of each. Samples were taken in 10,5 (x) 10,5 (x) 5 cm (551 cm3) plastic boxes. 
Sampling points were selected in a transect de 20 m, and for the random number sampling 
points were obtained. A total of 25 samples were taken per lagoon in every occasion, for a 
22 
 
total number of 200 samples in the whole of the study. Besides data temperature, relative 
humidity and CO2 of every point were taken with a multimeter (IAQ-CALC 8760-M-NP). 
Samples were carried to the Laboratory of Ecology and Systematic of Microarthropods 
at the Faculty of Sciences, UNAM, and processed by Berlese funnels during six days, the 
three first with natural light and the three last ones with a heat source (a 60 watt lamp). 
Collembola obtained were fixed in 75% ethanol, and semi-permanent preparations were 
realized in order to identify to genus and species level under the phase contrast microscope. 
 
 
Figure 1. Location of the sampling zone in Cozumel Island, Quitana Roo, México. 
 
Data analysis 
Shannon diversity index was calculated for site and sampling data. The comparison made 
between them was through "t" student test and the Bonferroni correction (α = 0,004) for 
multiple comparisons (Zar 2010; Magurran 1988). Pielou’s evenness and Simpson’s 
dominance indices were also calculated. Analyses were performed in software STATECOL 
ver. 1, 12 (Ludwing & Reynolds 1998). The effective number of species, as measure units of 
true diversity (D), it was calculated with Partition 3.0 software (Veech & Crist 2009), where 
species present the sameweight to its abundance (diversity of order 1, q = 1), or higher weight 
to dominant species (diversity of order 2, q = 2). 
The effect of mangrove species (R. mangle or A. nitida) and the date of sampling (four 
expeditions) on the density of springtails was evaluated through a multivariate analysis of 
23 
 
variance (MANOVA), differences were tested by post-hoc Tukey´s test. The relationships 
among the environmental parameters (temperature, relative humidity and CO2 
concentration), and the abundance of springtails was evaluated through multiple correlations. 
Data were normalized for (Zar 2010). Analyses were performed in Statistica 
software ver. 8.0 (Statsoft 2007). 
 
Results 
Abundance and diversity of springtails 
A total of 13 673 springtails were collected, belonging to 14 families, 33 genera and 53 
species (Fig. 2). Lepidocyrtus ca. floridensis occupied 15% of the total abundance, followed 
by Hemisotoma thermophila and Xenylla yucatana, with the 14% each; Proisotoma ca. bulba 
(13%), X. pseudomaritima (10%), Folsomina onychiurina and Sphaeridia serrata with about 
5%, the remaining species are under this percentage (Fig. 2). 
Into the most abundant species, only Lepidocyrtus ca. floridensis was collected during 
all the study, followed by Xenylla pseudomaritima and X. yucatana, that were found in the 
raining season and in March 2012; Proisotoma ca. bulba, Hemisotoma thermophila, 
Folsomia onychiurina and Sphaeridia serrata, were collected only during the rainy season 
(Table 1). 
Of the total species, 46 were recorded at Rhizophora mangle, and 13 are exclusive of 
this mangrove; in other hand, to Avicennia nitida these were found 41 species, 7 of them 
exclusive of this mangrove. In the case of the seasons, 13 species were found in the dry 
season (3 exclusive) and 50 during rains (40 exclusive). 
Result of diversity, evenness and dominance indices are present in Table 1, the 
vegetation of R. mangle, presents a higher Shannon diversity index values, but the less 
Simpson’s dominance, and lower Pielou’s evenness, in comparison with A. nitida. 
Nevertheless, comparing the Shannon diversity index values between communities 
significant differences were not found (t0.06, 52= 0.16 p>0.05). 
In the case of sampling date, specifically during the rainy season, a higher Shannon 
diversity value was registered, as well dominance; nevertheless, evenness was higher during 
dry season. Comparing Shannon diversity among seasons, meaningful differences among 
them were found (t0.06, 52= 7.99 p<0.05). 
24 
 
 
 
Figure. 2 Porcentage of collembula of mangrove in Punta Sur, Cozumel, Quintana Roo. Others include: 
Ceratophysella sp., Xenyllodes armatus, Brachystomella neomexicana, Friesea mirabilis, F. ca. polla, 
Paranura ca. nudifera, P. rooensis, Neanura muscorum, Pseudachorutes ca. rugatus, P. simplex, 
Pseudachorudina ca. texensis, Deuteraphorura ca. opa, Tullbergia sp., T. ca. duops, Mesaphorura yosiii, 
Proisotoma bulba, P. frisoni, P. ca. minuta, P. ca. japonalica, P. tenella, Cryptopygus sp. C. ca. benhami, 
Hemisotoma ca. termophila, Folsomia fimetaria, Isotomiella minor, Isotomurus atreus, Entomobrya ca. 
confusa, Sinella ca. alata, Seira ca. bipunctata 1, S. ca. bipunctata 2, Pseudosinella alba, P. ca. collina, P. ca. 
orba, P. octopunctata, P. violenta, Cyphoderus similis, Sphaeridia pumilis, Collophora ca. quadriculata, 
Stenognathellus denisi, Calvatomina rufescens, Dicyrtoma ca. mithra, Sphyroteca mucroserrata, S. ca. 
mucroserrata, Neelus sp., Megalothorax rapoporti and M. interruptus. 
 
For true diversity (D), Laguna Colombia it was 0.06 times higher than in Laguna Chuc 
Chacaab for diversity of order 1 (q= 1), while for diversity of order 2 (q=2) was only 0.02 
times higher. Estimations show that we can expect 3.62 more species for the Laguna 
Colombia and 2.62 for Chuc Chacaab. 
In the case of collecting season, q=1 was 2.66 times higher for the rainy than the dry 
season; and for q=2 was 1.04 higher. Estimation of expected species shows, 0.31 times more 
species in the dry season and 7.12 in the rainy season. 
 
Sphaeridia serrata
Lepidocyrtus floridensis
Folsomia onychiurina Hemisotoma thermophila
Proisotoma ca.. bulba
Xenylla yucatana
Xenylla pseudomaritima
Varios
24 %
5 %
15 %
5 % 14 %
13 %
14%
10 %
25 
 
Table 1. Abundance of springtails in Punta Sur, Cozumel (± s.d. Dr= dry season, Ra= rainy, I= Rhizophora mangle, II= Avicennia nitida, *= new records). 
Fecha de colecta April 2011 (Dr) Sep. 2011 (Ra) Nov. 2011 (Ra) March 2012 (Dr) Total 
Taxón / vegetación I II I II I II I II I II 
Hypogastruridae 
*Ceratophysella sp. 2 2 
*Xenylla pseudomaritima 24 26 1 143 64 2 68 1 169 158 
*X. yucatana 1877 40 3 3 1 920 3 
Odontellidae 
*Xenyllodes armatus 46 14 8 14 54 
Brachystomellidae 
*Brachystomella neomexicana 2 2 
Neanuridae 
Friesea mirabilis 113 5 118 
*F. ca. polla 12 12 
*Paranura ca. nudifera 7 7 
*P. rooensis 31 31 
Neanura muscorum 1 5 5 1 
Pseudachorutes ca. rugatus 13 2 15 
*P. simplex 56 62 18 28 74 90 
Pseudachorudina ca. texensis 2 5 7 
Onychiuridae 
*Deuteraphorura ca. opa 4 2 11 1 15 3 
*Tullbergia sp. 1 29 26 1 6 31 32 
*T. ca. duops 29 29 
26 
 
Continuation table 1 
Mesaphorura yosiii 1 1 10 1 11 
Isotomidae 
*Proisotoma bulba 39 10 39 10 
*P. ca. bulba 1 285 342 55 40 1 340 382 
P. frisoni 3 10 3 10 
*P. ca. minuta 1 1 
P. tenella 15 2 
P. sp. 2 15 
Cryptopygus sp. 5 5 
*C. ca. benhami 144 12 7 144 19 
*Hemisotoma thermophila 463 1 352 10 91 473 1 443 
*H. ca. thermophila 60 10 2 60 12 
*Folsomia fimetaria 6 6 
Folsomina onychiurina 450 203 29 27 479 230 
Isotomiella minor 7 262 24 116 10 378 41 
*Isotomurus atreus 1 1 2 1 3 
Entomobryidae 
*Entomobrya ca. confusa 22 26 1 22 27 
*Sinella ca. alata 1 1 
*Seira ca. bipunctata (1) 31 33 64 
*Seira ca. bipunctata (2) 7 2 2 7 
Lepidocyrtus ca. floridensis 2 652 396 665 175 3 145 1 322 716 
*Pseudosinella alba 22 22 
*P. ca. collina 68 24 1 69 24 
27 
 
Continuation table 1 
*P. ca. orba 24 33 4 6 28 39 
*P. octopunctata 6 30 107 14 113 44 
*P. violenta 9 9 9 9 
Cyphoderidae 
*Cyphoderus similis 71 16 45 11 15 116 42 
Sminthurididae 
Sphaeridia pumilis 94 251 6 130 100 381 
S. serrata 38 574 7 124 45 698 
Collophoridae 
*Collophora quadriculata 56 81 2 56 83 
Katiannidae 
*Stenognathellus denisi 14 5 2 12 16 17 
Dicyrtomidae 
*Calvatomina rufescens 27 56 18 14 1 45 71 
*Dicyrtoma ca. mithra 2 3 5 
Sminthuridae 
Sphyroteca mucroserrata 33 11 42 44 75 55 
*S. ca. mucroserrata 6 6 
Neelidae 
Neelus sp. 107 10 15 122 10 
Megalothorax rapoporti 65 19 3 1 68 20 
*M. interruptus 55 42 21 6 42 82 
Total 10 9 6 231 3 858 2435 879 10 241 8 686 4 987 
Density ind/m2 0.22±0.003 0.20±0.004 138±1 87±0.8 55±0.6 20±0.1 0.2±0.003 9±0.1 196±2 116±1 
28 
 
Effect of the seasonality and habitat in the density of springtails 
Diversity of springtails was higher (Table 2), but only few species presented a wide seasonal 
abundance, as Lepidocyrtus ca. floridensis that was collected during all the study, or X. 
pseudomaritima, X. yucatana and H. thermophila, collecting them in two or three dates 
(Table 3). 
 
 
Table 2- Collembola´s diversity, in Punta Sur, Cozumel. I= Rhizophora mangle, II= Avicennia nitida, S= 
Richness of species, H’= Shanon diversity, J’= Pielou Equatitivity, λ= Simpson dominance, Es= observed and 
estimated, Ep= expected. 
 I II Dry season Rainy 
S 46 41 13 50 
H’ 2.5 2.47 1.37 2.71 
J’ 0.65 0.66 0.53 0.69 
 λ